Monge 2018. Necesidad 2mm Encía Queratinizada en Implantes
Monge 2018. Necesidad 2mm Encía Queratinizada en Implantes
Monge 2018. Necesidad 2mm Encía Queratinizada en Implantes
* Department of Oral Surgery and Stomatology, ZMK School of Dental Medicine, University of
Bern, Switzerland
Corresponding Author:
One sentence summary: The presence of keratinized mucosa in erratic compliers is associated with
This is the author manuscript accepted for publication and has undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process, which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
10.1002/JPER.18-0471.
Disclaimer: The authors have no direct financial interests with the products and instruments listed in
the paper.
Abstract
Background: Given the fact that most patients are not regular compliers in supportive peri-implant
maintenance programs, it is of interest to examine the significance of the peri-implant soft tissue
Material and Methods: Based on an a priori statistical power calculation, a cross-sectional study was
conducted on erratic peri-implant maintenance compliers (< 2x/year) in order to examine the
significance of keratinized mucosa (KM) and gingival tissue (KT) on peri-implant and adjacent
periodontal conditions in implants restored ≥ 3 years. Seven clinical parameters were recorded around
implants and the adjacent buccal sites. Radiographic assessment was carried out using periapical X-
rays. In addition, a visual analog scale (VAS) was used to evaluate the impact of KM upon brushing
comfort. The case definition used for peri-implant diseases was in accordance with the 2017 world
workshop on the classification of periodontal and peri‐ implant diseases and conditions.
Results: Overall, 37 patients with 45 edentulous gaps restored with 66 implants and 90 adjacent teeth
were analyzed. On comparing a KM band of < 2 mm versus ≥ 2 mm, with the exception of
suppuration (p=0.6), all the clinical and radiographic parameters were significantly increased when
the KM band was < 2 mm (p ≤ 0.001). A significant correlation was observed between KM and KT
Conclusion: The presence of < 2 mm of KM around dental implants in erratic maintenance compliers
phenomenon independent of the keratinized tissue present in the adjacent dentition (NCT03501537).
Introduction
The morphological characteristics of the gingiva have been regarded as crucial for the integrity of the
periodontium.1 This claim is based on the fact that movable mucosa facilitates the penetration of
biofilm into the crevice, which in turn would trigger the activation of neutrophils and lymphocytes. 2
These would cause chronification of the inflammatory response, resulting in attachment loss. 3 Hence,
it has been advocated that an adequate zone of keratinized tissue (KT) with an attached area are
decisive in order to maintain the stability of the periodontal tissues. 4 This requirement is of lesser
The significance of keratinized mucosa (KM) bordering dental implants has not been without
controversy, and focused much debate especially during the 1990s.8-12 The reason for this academic
disagreement was mainly the fact that the vast majority of commercial dental implants at the time
were machined/turned designs which in turn may minimize biofilm accumulation when compared to
modified surfaces. This issue is of considerable significance, since plaque accumulation may lead to a
greater inflammatory infiltrate dominated by lymphocytes and plasmatic cells when compared to
natural teeth.13 In this regard, a meta-analysis of recent trials revealed statistically significant
differences in plaque index, modified gingival index, mucosal recession and attachment loss, with
results all favoring implants with a wide band of KM.14 In this sense, the lack of KM is positively
and ability to acquire adequate personal oral hygiene habits. In addition, the presence of KM around
dental implants has been shown to have an impact upon immunological parameters, with a negative
Supportive periodontal therapy (SPT) and peri-implant maintenance therapy (PIMT) have been shown
to be crucial to the longevity of both natural teeth19-23 and dental implants.24-29 In this regard, the
compliance rate has also been shown to potentially condition the development of biological
complications. Findings from a recent systematic review suggest that compliance with a biannual
PIMT program results in an approximately three-fold increased efficacy in the prevention of peri-
implant diseases. In agreement with this, clinical trials have underscored the importance of
professionally providing PIMT ≥ 2 times/year compared with less frequent recalls.24, 29 Nonetheless,
approximately 60% of all patients are either erratic compliers (< 2x/year) or non-compliers (0x/year),
and of these, roughly one out of five develop peri-implantitis.24 Given the fact that even in the absence
of adequate PIMT enrollment the majority of erratic compliers or non-compliers do not develop
pathological conditions characterized by progressive bone loss, it seems of interest to examine the
The present study thus assesses the significance of KM in erratic (< 2x/year) compliers. In addition,
an evaluation is made of the influence of the band of KM upon the peri-implant conditions in
A cross-sectional study was conducted in accordance with the Declaration of Helsinki on human
studies, following approval from the Ethics Committee of the University of Extremadura (Badajoz,
of 2018. The study was also registered and approved by www.clinicaltrials.gov (NCT03501537), and
Study population
All enrolled subjects had been consecutively evaluated with dental implants in function and a screw-
retained fixed prosthesis for a minimum of 36 months after final prosthesis delivery. All eligible
patients had to fall within the following definition of erratic compliance: not attending to a minimum
Patients were either contacted and invited to participate in a study to identify the peri-
implant/periodontal conditions or the evaluation was carried out during supportive periodontal/peri-
implant treatment performed in a Private Practice exclusive in Periodontics and Implant Dentistry
(CICOM | Periodoncia, Badajoz, Spain). The clinical, radiographic analyses were carried out by one
periodontist (AM) with more than 5 years involved in clinical research accredited by the American
Academy of Periodontology (ABP). The baseline x-rays at the time of prosthesis delivery were
retrospectively examined to exclude implants with excessive early peri-implant bone loss before
All included patients were informed – as part of the initial phase - to adhere to a supportive peri-
implant maintenance therapy program tailored to the risk profile. As such, patients with history of
periodontal disease were recommended to attend every 3-4 months and patients without history of
periodontal disease were suggested to comply every 5-6 months. Supportive periodontal/peri-implant
maintenance therapy was carried out by an experienced hygienist (>5 years of expertise) with plastic
on the use of inter-proximal brush and floss with stiffened end to cleanse the inter-proximal areas.
The prescreening was performed by reviewing the internal records. An a priori statistical power
analysis was carried out to calculate the sample size. Overall, 37 patients were determined to be
recruited assuming an intra-class correlation coefficient of 0.25. All the eligible patients were
consecutively invited when attending to other departments at the same practice for other
reasons/concerns (i.e., prosthodontics, oral & maxillofacial surgery and orthodontist) or when
period, 3 patients resulted to be current smokers and hence were invited to adhere to a regular
Eligibility criteria
The following inclusion criteria were applied: implant-supported single-crown and fixed prostheses,
patients aged 18-80 years; non-smokers; absence of infectious disease at the time of implant
placement or during the maintenance program; absence of systemic disorders or medication known to
alter bone metabolism; partially edentulous patients with gaps associated to at least one mesial and
one distal adjacent tooth, without sign of active periodontal disease and with or without a history of
chronic periodontitis. Subjects in turn were excluded for the following reasons: pregnancy; lactation;
past or present heavy smoking; uncontrolled medical conditions such as diabetes mellitus; inadequate
Periodontal and Peri‐Implant Diseases and Conditions 30, the diagnosis of health required:
No bone loss beyond crestal bone level changes resulting from initial bone remodeling.
The diagnosis of peri-implant mucositis in turn was established from the following:
No bone loss beyond crestal bone level changes resulting from initial bone remodeling.
Lastly, the diagnosis of peri-implantitis in turn was established from the following:
Bone level ≥ 3 mm apical to the most coronal portion of the intraosseous part of the implant.
Clinical assessment
The following clinical parameters and indexes were recorded at the buccal sites of the studied
Plaque index (PI) scored from 0-3 according to the visibility and severity of plaque
accumulation.32
Keratinized mucosa (KM) around dental implants, measured from the free mucosal margin to
the mucogingival junction at the mid-buccal, mesial and distal line-angles, and recorded to the
nearest mm using a North Carolina Probe. If unclear, Lugol’s iodine was used to stain the
mucosa to better discern the mucogingival margin. The firm and resilient KM was identified
Keratinized gingival tissue (KT) around natural dentition, measured from the free mucosal
margin to the mucogingival junction at the mid-buccal, mesial and distal line-angles, and
recorded to the nearest mm using a North Carolina Probe. If unclear, Lugol’s iodine was used
Vestibular depth (VD) measured using a North Caroline Probe from the mucosal margin to
the point of greatest concavity of the mucobuccal fold while a retracting with a bilateral
retractor. Vestibular depth was rated as shallow (< 4 mm) or deep (≤ 4 mm).
Suppuration (SUP) around implants and teeth, recorded by a dichotomous (1/0) scale using a
Moreover, the patients were interviewed by one examiner (AM) using a visual analog scale (VAS) to
assess brushing comfort prior to assess the clinical condition to minimize bias. The VAS recorded a
characteristic (comfort) ranging across a continuum of values, and which is not easy to measure
directly. The score ranged from 0 (maximum discomfort) to 100 (maximum comfort) and was
One examiner (AM) assessed the radiographic bone level (intra-rater Cohen kappa value >90% -
almost perfect). Peri-implant radiographic bone loss (MBL) was determined by taking linear
measurements from the most mesial and distal point of the implant platform to the crestal bone on
each peri-apical radiograph, corrected according to the known height and width of each implant using
Statistical analysis
A priori statistical power analysis was performed assuming an intra-class correlation coefficient (ICC)
of 0.25, based on a previous study.33 The Kolmogorov-Smirnov test was applied to assess normality
between the parameters KM and KT. Pearson’s correlation coefficient was used to assess the
correlations between the presence/lack of KM in the edentulous gap and the other clinical and
radiographic parameters or KT of the adjacent teeth. The Mann-Whitney U-test was applied to
validate the homogeneity of the clinical parameters for teeth and implants. In the event of a non-
homogeneous distribution, we used the Spearman correlation test. The Kruskal-Wallis test was
The inferential analysis involved estimation by generalized estimating equations (GEEs) of multilevel
logistic regression models. Calculations were made to assess any parameter recorded at implant-level
Results
Study population
Based on the a priori sample size calculation, 37 Caucasian patients (37.6% females, 32.4% males;
mean age: 49.9±12.9 years) with 45 edentulous gaps restored with 66 implants (mean follow-up:
5.73±2.89 years) and 90 adjacent teeth were analyzed. Of these, 30 (81.1%), 6 (16.2%) and 1 (16.2%)
29.7%), 7 (18.9%) and 1 (2.7%) patients carried 1, 2, 3 and 5 implants, respectively. In turn, 30
(81.1%), 6 (16.2%) and 1 (16.2%) patients respectively had 2, 4 and 6 teeth examined. A total of 196
Overall, 8 (21.62%) out of the 37 patients presented with active periodontal disease (residual pockets
≥5mm with bleeding on probing), 16 (43.24%) were controlled individuals with history of chronic
periodontitis (no residual pockets ≥5mm) and 13 (35.14%) were not diagnosed with active or history
of periodontitis (no pockets ≥5mm). Regarding the level of radiographic attachment loss, 5.40% (2
patients) presented advanced loss of support in the dentition (>50%), 24.33% (9 patients) with
moderate loss (30%-50%) and 70.27% (26 patients) with mild attachment loss (<30%). The grade of
attachment loss was neither associated with the width of the KT and/nor the KM (p=0.22).
Overall, 45 edentulous gaps were analyzed of which, 26 were assessed in the posterior mandible,
followed by 17 in the posterior maxilla and a vast minority in the anterior regions (2). According to
the location, the posterior mandible was the most common area displaying <2mm of KM (77%), while
this was less frequently in the other locations. In this area, 53.8% accounted for <2mm of KM, while
in the posterior maxilla 17.6%. On the other side, 82.4% and 100% of the posterior and anterior
maxillary sites, respectively, and 46.2% and 0% in the posterior and anterior mandibular sites,
The vast majority of the implants examined presenting a band of ≥2mm of KM displayed mucosal
attachment (92%), while AM could not be found in implants with <2mm of KM (0%). When
comparing a KM band of < 2 mm versus ≥ 2 mm, with the exception of SUP, all the clinical and
1). Moreover, KM was positively associated with VD. A lack of KM was significantly associated with
peri-implantitis (p<0.001).
The width of the KM band was significantly associated (p<0.001) with the health and peri-implantitis
rates, but not with peri-implant mucositis (Figure 2). Interestingly, under the presence of KM, on
comparing a band ranging from 0 to 1.99mm versus ≥ 2 mm, only mucositis was found to be
significantly greater (p<0.05) in the < 2 mm group. Neither peri-implantitis nor healthy implants
In the presence of a KM band of < 2 mm, the VAS score decreased significantly (p<0.001).
Interestingly, when the mean KM band was 2.5 mm, all the patients reported maximum comfort
(VAS=100).
The mean KM band width was 2.35±1.83 mm (range 0-6.33 mm), with a median of 2.2 mm. In 40%
of the edentulous implant-supported sites, the mean KM band was < 2 mm, while the remaining 60%
presented a KM band width of ≥ 2 mm. On the other hand, the KT band width was substantially
greater, with a mean value of 3.49±1.12 mm (range 1-6.50 mm) and a median of 3.50 mm.
The correlation between KM and KT of the adjacent teeth was statistically significant (p=0.002;
r=0.55). In other words, in scenarios characterized by a lack or narrow band of KM, the KT band of
exhibited that the correlation was strongly associated by the locations in the posterior maxilla (r=0.56;
p=0.018), while not in the posterior mandibular sites (r=0.07; p=0.71). Namely, in the posterior
mandible, the KM was significantly lower compared to adjacent KT sites, while in the posterior
maxilla, KM was significantly associated with the KT of the adjacent teeth (median KT: 4.00mm;
median KM: 3.67). However, in none of the cases was a lack of KM associated with a lack of KT of
any of the adjacent teeth. This underscore that the lack of KM constitutes a site-specific phenomenon.
The KM was shown to be wider at the mesial (p=0.01) and distal line angles (p=0.01) of the implants,
and significantly narrower at the medial sites. Nevertheless, on considering the median values, KM
was equal at the three buccal sites, those measuring ≥ 2 mm ranging from 60.6% to 61.5%. Again,
significantly greater values were recorded for PPD, PI and MBL at sites measuring < 2 mm. In
relation to mBI, although a positive trend was observed, statistical significance was not reached
(p=0.05). The statistical relationship became stronger at DB (disto-buccal) sites for all the clinical and
The periodontal condition was seen to be independent of KM band width. However, mBI increased
A positive correlation was found among PPD, mBI and PI in the assessed implants and adjacent teeth
(r=0.5) (Table 2 and Figure 3). Nevertheless, this fact was inconsistent with the presence (and width)
or absence of KM or KT.
Principal findings
There has been much debate on the potential impact of KM upon peri-implant conditions.
Based on previous clinical trials, its influence in relation to peri-implant bone loss is
erythema, bleeding on probing and tumefaction. The great disparity of the existing evidence
is referred to one predominant aspect. Data found in the literature suggests no association
between KM and peri-implant conditions in patients with adequate plaque control.39 Along
these lines, it is worth mentioning that implant/restorative surface topography might play a
role on biofilm development.40 Our own results partially concur with this, since in erratic
maintenance compliers, a KM band width of < 2 mm was significantly associated with more
which in turn may decrease patient ability to correctly implement personalized oral hygiene
measures.
On the other hand, it has been shown that a lack of KM is a site-specific condition.
adjacent teeth. In other words, when the KT band of the adjacent teeth is narrow, it increases
the probability of a narrow or inexistent KM on the buccal site of the implants. In any case, a
lack of KM always occurs in the presence of KT. Along these lines, it is important to note
that in scenarios characterized by a lack of KM, mBI was found to be greater at sites adjacent
Our clinical findings support the view that KM around dental implants in erratic maintenance
compliers seems necessary for maintaining peri-implant health, and are consistent with
previously reported pre-clinical9, 41 and clinical observations34-38. Moreover, recent data have
evidenced the influence of the width of KM upon the peri-implant clinical parameters in
relation to the onset and resolution of experimental peri-mucositis in humans.42 The data are
not fully consistent throughout the literature, however.8, 10, 43, 44 It has been speculated that
these disagreements are partly due to the patient selection process involved. For instance, it
must be noted that the patients enrolled in the aforementioned studies followed adequate
comparison, our cohort of patients were treated and restored in private practice and were
erratic maintenance compliers. Hence, we partially concur with the findings indicating the
KM45. In the absence of KM, there is a mobile lining mucosa rich in elastic fibers and poor in
collagen.46 This agrees with the findings of a recent cross-sectional comparative study in
which implant sites with a KM band width of < 2 mm were found to be more prone to
pain threshold, brushing strength, mucosal thickness and other anatomy-related factors may
The positive association between KM and VD is of key importance, since it implies that a
shallow VD could interfere with proper oral hygiene techniques, thus leading to more plaque
accumulation. This finding is in agreement with a previous clinical study reporting the
association between VD and a lack of KM, and also increased bone loss and mucosal
Although a correlation was observed between KM and KT, a complete absence of KM was
not associated with a lack of KT - thus defining the former as a site-specific condition. This
critical finding suggests that there is a remodeling of soft tissues in the same way as there is a
Our study has a number of limitations. Firstly, a number of variables were not accounted for, such as
the width of KM/KT on the lingual aspect, keratinized tissue thickness or mucosal/gingival recession.
However, it must be mentioned that for the diagnosis of peri-implant conditions, the lingual sites
considered had to be bordered by sufficient KM. Because of the study design involved, a cause-effect
relationship cannot be claimed between peri-implant clinical parameters and KM. In this sense, it
should be highlighted that future studies should monitor the peri-implant clinical and radiographic
Furthermore, it would be of particular interest to evaluate the dynamics of the band of KM according
to the peri-implant condition. Moreover, it must be noted that these findings are not applicable to
good maintenance compliers, where conflicting results have been reported regarding the significance
of KM.
Conclusion
The presence of < 2 mm of KM around dental implants in erratic maintenance compliers seems to be
Acknowledgments
The authors wish to acknowledge the FEDICOM Foundation (Badajoz, Spain) for financial support of
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Figure 1. Clinical and radiographic parameters according to the width of the band of keratinized
mucosa (<2mm)/≥2mm)
Tables
Table 1. Descriptive analysis of the clinical and radiographic parameters according to the width of
keratinized mucosa.
Keratinized mucosa
Keratinized mucosa
Differential r (p-value)
<2 mm ≥2 mm p-value
coefficient
n 26 40
PPD (mm) 4.86 ± 1.06 (5.00) 3.65 ± 1.06 (3.33) -1.21 ± 0.28 <0.001*** -0.57
(p<0.001***)
mBI 1.15 ± 0.69 (1.17) 0.46 ± 0.57 (0.17) -0.69 ± 0.17 <0.001*** -0.54
(p<0.001***)
(p=0.463)
PI 1.08 ± 0.86 (1.00) 0.28 ± 0.41 (0.00) -0.79 ± 0.21 <0.001*** -0.60
(p<0.001***)
MBL (mm) 2.03 ± 1.65 (2.10) 0.64 ± 0.93 (0.20) -1.39 ± 0.41 0.001** -0.55
(p<0.001***)
VAS (%) 53.8 ± 30.7 (60.0) 97.0 ± 8.5 (100.0) 43.2 ± 6.49 <0.001*** 0.703
(p<0.001***)
Implant diagnosis
adjacent dentition.
Implants